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Bacterial System for Alginate Uptake and Degradation

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Alginates: Biology and Applications

Part of the book series: Microbiology Monographs ((MICROMONO,volume 13))

Abstract

Most alginate-assimilating bacteria secrete degrading enzymes, i.e., alginate lyases, into the extracellular fraction or periplasm, and incorporate the resultant alginate oligosaccharides through their cytoplasmic membrane. The Gram-negative bacterium Sphingomonas sp. A1 can directly incorporate the polysaccharide into the cytoplasm, without degradation, through a mouthlike pit on the cell surface, periplasmic binding proteins, and an ATP-binding cassette importer in the cytoplasmic membrane. This uptake system (superchannel) is distinct from channels or transporters responsible for importing low molecular weight substrates. The constituent proteins are inducibly expressed and organized at the superchannel when flagellin homologues, as cell surface receptors, recognize the external alginate. Cytoplasmic alginate lyases with different substrate specificities and action modes help degrade the alginate into monosaccharides. The strain A1 superchannel can be transplanted to other sphingomonads through membrane engineering. This chapter reviews the bacterial system for alginate uptake and degradation by considering the structure and function of each molecule in the superchannel.

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References

  • Aizawa S-I (1996) Flageller assembly in Salmonella typhimurium. Mol Microbiol 19:1–5

    Article  PubMed  CAS  Google Scholar 

  • Akiyama H, Endo T, Nakakita R, Murata K, Yonemoto Y, Okayama K (1992) Effect of depolymerized alginates on the growth of bifidobacteria. Biosci Biotechnol Biochem 56:355–356

    Article  PubMed  CAS  Google Scholar 

  • Andrews NW, Abrams CK, Slatin SL, Griffiths G (1990) A T. cruzi-secreted protein immunologically related to the complement component C9: evidence for membrane pore-forming activity at low pH. Cell 61:1277–1287

    Article  PubMed  CAS  Google Scholar 

  • Aso Y, Miyamoto Y, Harada KM, Momma K, Kawai S, Hashimoto W, Mikami B, Murata K (2006) Engineered membrane superchannel improves bioremediation potential of dioxin-degrading bacteria. Nat Biotechnol 24:188–189

    Article  PubMed  CAS  Google Scholar 

  • Boos W, Shuman H (1998) Maltose/maltodextrin system of Escherichia coli: transport, metabolism, and regulation. Microbiol Mol Biol Rev 62:204–229

    PubMed  CAS  Google Scholar 

  • Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, Gwinn ML, Dodson RJ, Deboy RT, Durkin AS, Kolonay JF, Madupu R, Daugherty S, Brinkac L, Beanan MJ, Haft DH, Nelson WC, Davidsen T, Zafar N, Zhou L, Liu J, Yuan Q, Khouri H, Fedorova N, Tran B, Russell D, Berry K, Utterback T, Van Aken SE, Feldblyum TV, D’Ascenzo M, Deng WL, Ramos AR, Alfano JR, Cartinhour S, Chatterjee AK, Delaney TP, Lazarowitz SG, Martin GB, Schneider DJ, Tang X, Bender CL, White O, Fraser CM, Collmer A (2003) The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci U S A 100:10181–10186

    Article  PubMed  CAS  Google Scholar 

  • Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322

    Article  PubMed  CAS  Google Scholar 

  • Coulton JW, Mason P, Cameron DR, Carmel G, Jean R, Rode HN (1986) Protein fusions of β-galactosidase to the ferrichrome-iron receptor of Escherichia coli K-12. J Bacteriol 165:181–192

    PubMed  CAS  Google Scholar 

  • Davidson AL, Chen J (2004) ATP-binding cassette transporters in bacteria. Annu Rev Biochem 73:241–268

    Article  PubMed  CAS  Google Scholar 

  • Gacesa P (1988) Alginates. Carbohydr Polym 8:161–182

    Article  CAS  Google Scholar 

  • Gray KA, Zhao L, Emptage M (2006) Bioethanol. Curr Opin Chem Biol 10:141–146

    Article  PubMed  CAS  Google Scholar 

  • Hanley SZ, Pappin DJ, Rahman D, White AJ, Elborough KM, Slabas AR (1999) Re-evaluation of the primary structure of Ralstonia eutropha phasin and implications for polyhydroxyalkanoic acid granule binding. FEBS Lett 447:99–105

    Article  PubMed  CAS  Google Scholar 

  • Hashimoto W, Miyake O, Momma K, Kawai S, Murata K (2000) Molecular identification of oligoalginate lyase of Sphingomonas sp. strain A1 as one of the enzymes required for complete depolymerization of alginate. J Bacteriol 182:4572–4577

    Article  PubMed  CAS  Google Scholar 

  • Hashimoto W, Mishima Y, Miyake O, Nankai H, Momma K, Murata K (2002) Biodegradation of alginate, xanthan, and gellan. In: Steinbüchel, A Biopolymers, polysaccharides I, vol 7. Wiley, Weinheim, pp 175–199

    Google Scholar 

  • Hashimoto W, He J, Wada Y, Nankai H, Mikami B, Murata K (2005a) Proteomics-based identification of outer-membrane proteins responsible for import of macromolecules in Sphingomonas sp. A1: alginate-binding flagellin on the cell surface. Biochemistry 44:13783–13794

    Article  CAS  Google Scholar 

  • Hashimoto W, Miyake O, Ochiai A, Murata K (2005b) Molecular identification of Sphingomonas sp. A1 alginate lyase (A1-IV′) as a member of novel polysaccharide lyase family 15 and implications in alginate lyase evolution. J Biosci Bioeng 99:48–54

    Article  CAS  Google Scholar 

  • Hashimoto W, Momma K, Maruyama Y, Yamasaki M, Mikami B, Murata K (2005c) Structure and function of bacterial super-biosystem responsible for import and depolymerization of macromolecules. Biosci Biotechnol Biochem 69:673–692

    Article  CAS  Google Scholar 

  • Harada KM, Aso Y, Hashimoto W, Mikami B, Murata K (2006) Sequence and analysis of the 46.6-kb plasmid pA1 from Sphingomonas sp. A1 that corresponds to the typical IncP-1β plasmid backbone without any accessory gene. Plasmid 56:11–23

    Article  PubMed  CAS  Google Scholar 

  • Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, Goodlett DR, Eng JK, Akira S, Underhill DM, Aderem A (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410:1099–1103

    Article  PubMed  CAS  Google Scholar 

  • He J, Ochiai A, Fukuda Y, Hashimoto W, Murata K (2008) A putative lipoprotein of Sphingomonas sp. A1 binds alginate rather than a lipid moiety. FEMS Microbiol Lett 288:221–226

    Article  PubMed  CAS  Google Scholar 

  • He J, Nankai H, Hashimoto W, Murata K (2004) Molecular identification and characterization of an alginate-binding protein on the cell surface of Sphingomonas sp. A1. Biochem Biophys Res Commun 322:712–717

    Article  PubMed  CAS  Google Scholar 

  • Hisano T, Kimura N, Hashimoto W, Murata K (1996) Pit structure on bacterial cell surface. Biochem Biophys Res Commun 220:979–982

    Article  PubMed  CAS  Google Scholar 

  • Iwamoto M, Kurachi M, Nakashima T, Kim D, Yamaguchi K, Oda T, Iwamoto Y, Muramatsu T (2005) Structure-activity relationship of alginate oligosaccharides in the induction of cytokine production from RAW264.7 cells. FEBS Lett 579:4423–4429

    Article  PubMed  CAS  Google Scholar 

  • Iwamoto Y, Xu X, Tamura T, Oda T, Muramatsu T (2003) Enzymatically depolymerized alginate oligomers that cause cytotoxic cytokine production in human mononuclear cells Biosci Biotechnol Biochem 67:258–263

    Article  PubMed  CAS  Google Scholar 

  • Jensen A (1993) Present and future needs for algae and algal polysaccharides. Hydrobiologica 260–261:15

    Google Scholar 

  • Kawada A, Hiura N, Shiraiwa M, Tajima S, Hiruma M, Hara K, Ishibashi A, Takahara H (1997) Stimulation of human keratinocyte growth by alginate oligosaccharides, a possible co-factor for epidermal growth factor in cell culture. FEBS Lett 408:43–46

    Article  PubMed  CAS  Google Scholar 

  • Kawada A, Hiura N, Tajima S, Takahara H (1999) Alginate oligosaccharides stimulate VEGF-mediated growth and migration of human endothelial cells. Arch Dermatol Res 291:542–547

    Article  PubMed  CAS  Google Scholar 

  • Kawasaki S, Moriguchi R, Sekiya K, Nakai T, Ono E, Kume K, Kawahara K (1994) The cell envelope structure of the lipopolysaccharide-lacking gram-negative bacterium Sphingomonas paucimobilis. J Bacteriol 176:284–290

    PubMed  CAS  Google Scholar 

  • Kinjo Y, Wu D, Kim G, Xing GW, Poles MA, Ho DD, Tsuji M, Kawahara K, Wong CH, Kronenberg M (2005) Recognition of bacterial glycosphingolipids by natural killer T cells. Nature 434:520–525

    Article  PubMed  CAS  Google Scholar 

  • Koedding J, Howard P, Kaufmann L, Polzer P, Lustig A, Welte W (2004) Dimerization of TonB is not essential for its binding to the outer membrane siderophore receptor FhuA of Escherichia coli. J Biol Chem 279:9978–9986

    Article  PubMed  CAS  Google Scholar 

  • Kurachi M, Nakashima T, Miyajima C, Iwamoto Y, Muramatsu T, Yamaguchi K, Oda T (2005) Comparison of the activities of various alginates to induce TNF-α secretion in RAW264.7 cells. J Infect Chemother 11:199–203

    Article  PubMed  CAS  Google Scholar 

  • Larsen RA, Thomas MG, Postle K (1999) Proton motive force, ExbB and ligand-bound FepA drive conformational changes in TonB. Mol Microbiol 31:1809–18024

    Article  PubMed  CAS  Google Scholar 

  • Leiman PG, Chipman PR, Kostyuchenko VA, Mesyanzhinov VV, Rossmann MG (2004) Three-dimensional rearrangement of proteins in the tail of bacteriophage T4 on infection of its host. Cell 118:419–429

    Article  PubMed  CAS  Google Scholar 

  • Linker A, Meyer K, Hoffman P (1956) The production of unsaturated uronides by bacterial hyaluronidases. J Biol Chem 219:13–25

    PubMed  CAS  Google Scholar 

  • Llanes F, Ryan DH, Marchessault RH (2000) Magnetic nanostructured composites using alginates of different M/G ratios as polymeric matrix. Int J Biol Macromol 27:35–40

    Article  PubMed  CAS  Google Scholar 

  • Lundrigan MD, Kadner RJ (1986) Nucleotide sequence of the gene for the ferrienterochelin receptor FepA in Escherichia coli. Homology among outer membrane receptors that interact with TonB. J Biol Chem 261:10797–10801

    PubMed  CAS  Google Scholar 

  • Maruyama Y, Momma M, Mikami B, Hashimoto W, Murata K (2008) Crystal structure of a novel bacterial cell-surface flagellin binding to a polysaccharide. Biochemistry 47:1393–1402

    Article  PubMed  CAS  Google Scholar 

  • May TB, Chakrabarty AM (1994) Pseudomonas aeruginosa: genes and enzymes of alginate synthesis. Trends Microbiol 2:151–157

    Article  PubMed  CAS  Google Scholar 

  • Mikami B, Suzuki S, Yoon H-J, Miyake O, Hashimoto W, Murata K (2002) X-ray structural analysis of alginate lyase A1-III mutants/substrate complexes: activation of a catalytic tyrosine residue by a flexible lid loop. Acta Crystallogr A 58:C271

    Article  Google Scholar 

  • Mishima Y, Momma K, Hashimoto W, Mikami B, Murata K (2001) Crystallization and preliminary X-ray analysis of AlgS, a bacterial ATP-binding-cassette (ABC) protein specific to macromolecule import. Acta Crystallogr D Biol Crystallogr 57:884–885

    Article  PubMed  CAS  Google Scholar 

  • Mishima Y, Momma K, Hashimoto W, Mikami B, Murata K (2003) Crystal structure of AlgQ2, a macromolecule (alginate)-binding protein of Sphingomonas sp. A1, complexed with an alginate tetrasaccharide at 1.6-Ã… resolution. J Biol Chem 278:6552–6559

    Article  PubMed  CAS  Google Scholar 

  • Miyake O, Hashimoto W, Murata K (2003) An exotype alginate lyase in Sphingomonas sp. A1: overexpression in Escherichia coli, purification, and characterization of alginate lyase IV (A1-IV). Protein Expr Purif 29:33–41

    Article  PubMed  CAS  Google Scholar 

  • Miyake O, Ochiai A, Hashimoto W, Murata K (2004) Origin and diversity of alginate lyases of families PL-5 and -7 in Sphingomonas sp. strain A1. J Bacteriol 186:2891–2896

    Article  PubMed  CAS  Google Scholar 

  • Momma K, Mikami B, Mishima Y, Hashimoto W, Murata K (2002) Crystal structure of AlgQ2, a macromolecule (alginate)-binding protein of Sphingomonas sp. A1 at 2.0Ã… resolution. J Mol Biol 316:1061–1069

    Article  CAS  Google Scholar 

  • Momma K, Mishima Y, Hashimoto W, Mikami B, Murata K (2005) Direct evidence for Sphingomonas sp. A1: periplasmic proteins as macromolecule-binding proteins associated with ABC transporter: molecular insights into alginate transport in the periplasm. Biochemistry 44:5053–5064

    Article  PubMed  CAS  Google Scholar 

  • Momma K, Okamoto M, Mishima Y, Mori S, Hashimoto W, Murata K (2000) A novel bacterial ATP-binding cassette (ABC) transporter system that allows uptake of macromolecules. J Bacteriol 182:3998–4004

    Article  PubMed  CAS  Google Scholar 

  • Moreno S, Nájera R, Guzmán J, Soberón-Chávez G, Espín G (1998) Role of alternative sigma factor algU in encystment of Azotobacter vinelandii. J Bacteriol 180:2766–2769

    PubMed  CAS  Google Scholar 

  • Murata K, Inose T, Hisano T, Abe S, Yonemoto Y, Yamashita T, Takagi M, Sakaguchi K, Kimura A, Imanaka T (1993) Bacterial alginate lyase: enzymology, genetics and application. J Ferment Bioeng 76:427–437

    Article  CAS  Google Scholar 

  • Murata K, Kawai S, Mikami B, Hashimoto W (2008) Superchannel of bacteria: biological significance and new horizons. Biosci Biotechnol Biochem 72:265–277

    Article  PubMed  CAS  Google Scholar 

  • Noronha FS, Cruz JS, Beirao PS, Horta MF (2000) Macrophage damage by Leishmania amazonensis cytolysin: evidence of pore formation on cell membrane. Infect Immun 68:4578–4584

    Article  PubMed  CAS  Google Scholar 

  • Ochiai A, Hashimoto W, Murata K (2006) A biosystem for alginate metabolism in Agrobacterium tumefaciens strain C58: molecular identification of Atu3025 as an exotype family PL-15 alginate lyase. Res Microbiol 157:642–649

    Article  PubMed  CAS  Google Scholar 

  • Ochiai A, Takase R, Hashimoto W, Murata K (2008) Molecular identification of reductase involved in detoxifying alpha-keto acid derived from alginate monosaccharide. Abstract for the annual meeting of the Society for Biotechnology, Japan, page 182

    Google Scholar 

  • Ogura K, Yamasaki M, Mikami B, Hashimoto W, Murata K (2008) Substrate recognition by family 7 alginate lyase from Sphingomonas sp. A1. J Mol Biol 380:373–385

    Article  PubMed  CAS  Google Scholar 

  • Oldham ML, Khare D, Quiocho FA, Davidson AL, Chen J (2007) Crystal structure of a catalytic intermediate of the maltose transporter. Nature 450:515–521

    Article  PubMed  CAS  Google Scholar 

  • Preiss J, Ashwell G (1962) Alginic acid metabolism in bacteria. I. Enzymatic formation of unsaturated oligosaccharides and 4-deoxy-L-erythro-5-hexoseulose uronic acid. J Biol Chem 237:309–316

    PubMed  CAS  Google Scholar 

  • Pressler U, Staudenmaier H, Zimmermann L, Braun V (1988) Genetics of the iron dicitrate transport system of Escherichia coli. J Bacteriol 170:2716–2724

    PubMed  CAS  Google Scholar 

  • Quiocho FA, Spurlino JC, Rodseth LE (1997) Extensive features of tight oligosaccharide binding revealed in high-resolution structures of the maltodextrin transport/chemosensory receptor. Structure 5:997–1015

    Article  PubMed  CAS  Google Scholar 

  • Remminghorst U, Rehm BH (2006) Bacterial alginates: from biosynthesis to applications. Biotechnol Lett 28:1701–1712

    Article  PubMed  CAS  Google Scholar 

  • Sakakibara H, Tamura T, Suzuki T, Hisano T, Abe S, Murata K (2002) Preparation and properties of alginate lyase modified with poly(ethylene glycol). J Pharm Sci 91:1191–1199

    Article  PubMed  CAS  Google Scholar 

  • Schweizer HP, Boring III JR (1973) Antiphagocytic effect of slime from a mucoid strain of Pseudomonas aeruginosa. Infect Immun 3:762–767

    Google Scholar 

  • Shimizu M (1999) Modulation of intestinal functions by food substances. Nahrung 43:154–158

    Article  PubMed  CAS  Google Scholar 

  • Sreeram KJ, Shrivastava HY, Nair BU (2004) Studies on the nature of interaction of iron(III) with alginates. Biochim Biophys Acta 1670:121–125

    PubMed  CAS  Google Scholar 

  • Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, Brinkman FSL, Hufnagle WO, Kowalik DJ, Lagrou M, Garber RL, Goltry L, Tolentino E, Westbrock-Wadman S, Yuan Y, Brody LL, Coulter SN, Folger KR, Kas A, Larbig K, Lim R, Smith K, Spencer D, Wong GK-S, Wu Z, Paulsen IT, Reizer J, Saier MH, Hancock REW, Lory S, Olson MV (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959–964

    Article  PubMed  CAS  Google Scholar 

  • Sugawara N, Tomita T, Sato T, Kamio Y (1999) Assembly of Staphylococcus aureus leukocidin into a pore-forming ring-shaped oligomer on human polymorphonuclear leukocytes and rabbit erythrocytes. Biosci Biotechnol Biochem 63:884–891

    Article  PubMed  CAS  Google Scholar 

  • Takeuchi M, Hamana K, Hiraishi A (2001) Proposal of the genus Sphingomonas sensu stricto and three new genera, Sphingobium, Novosphingobium and Sphingopyxis, on the basis of phylogenetic and chemotaxonomic analyses. Int J Syst Evol Microbiol 51:1405–1417

    PubMed  CAS  Google Scholar 

  • Turley EV, Noble PW, Bourguignon LYW (2002) Signaling properties of hyaluronan receptors. J Biol Chem 277:4589–4592

    Article  PubMed  CAS  Google Scholar 

  • Walker JC (1987) Was the Archaean biosphere upside down? Nature 329:710–712

    Article  PubMed  CAS  Google Scholar 

  • White DC, Sutton SD, Ringelberg DB (1996) The genus Sphingomonas: physiology and ecology. Curr Opin Biotechnol 7:301–306

    Article  PubMed  CAS  Google Scholar 

  • Wittich RM, Wilkes H, Sinnwell V, Francke W, Fortnagel P (1992) Metabolism of dibenzo-p-dioxin by Sphingomonas sp. strain RW1. Appl Environ Microbiol 58:1005–1010

    PubMed  CAS  Google Scholar 

  • Wong TY, Preston LA, Schiller NL (2000) Alginate lyase: review of major sources and enzyme characteristics, structure-function analysis, biological roles, and applications. Annu Rev Microbiol 54:289–340

    Article  PubMed  CAS  Google Scholar 

  • Yamasaki M, Ogura K, Hashimoto W, Mikami B, Murata K (2005) A structural basis for depolymerization of alginate by polysaccharide lyase family-7. J Mol Biol 352:11–21

    Article  PubMed  CAS  Google Scholar 

  • Yonekura K, Maki-Yonekura S, Namba K (2003) Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424:643–650

    Article  PubMed  CAS  Google Scholar 

  • Yoon H-J, Mikami B, Hashimoto W, Murata K (1999) Crystal structure of alginate lyase A1-III from Sphingomonas species A1 at 1.78 Ã… resolution. J Mol Biol 290:505–514

    Article  PubMed  CAS  Google Scholar 

  • Yoon H-J, Hashimoto W, Miyake O, Okamoto M, Mikami B, Murata K (2000) Overexpression in Escherichia coli, purification, and characterization of Sphingomonas sp. A1 alginate lyases. Protein Expr Purif 19:84–90

    Article  PubMed  CAS  Google Scholar 

  • Yoon H-J, Hashimoto W, Miyake O, Murata K, Mikami B (2001) Crystal structure of alginate lyase A1-III complexed with trisaccharide product at 2.0 Ã… resolution. J Mol Biol 307:9–16

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by Grants-in-Aid (to K.M., B.M., and W.H.) and by the Targeted Proteins Research Program (to W.H.) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan. Part of this work was also supported by the Program of Basic Research Activities for Innovative Biosciences (PROBRAIN) of Japan (to K.M.).

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Authors and Affiliations

  1. Laboratory of Basic and Applied Molecular Biotechnology, Graduate School of Agriculture, Kyoto University, Uji, Kyoto, 611-0011, Japan

    Wataru Hashimoto, Yukie Maruyama, Takafumi Itoh & Kousaku Murata

  2. Laboratory of Applied Structural Biology, Graduate School of Agriculture, Kyoto University, Uji, Kyoto, 611-0011, Japan

    Bunzo Mikami

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  1. Wataru Hashimoto
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  2. Yukie Maruyama
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  3. Takafumi Itoh
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  4. Bunzo Mikami
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  5. Kousaku Murata
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Correspondence to Kousaku Murata .

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    Hashimoto, W., Maruyama, Y., Itoh, T., Mikami, B., Murata, K. (2009). Bacterial System for Alginate Uptake and Degradation. In: Rehm, B. (eds) Alginates: Biology and Applications. Microbiology Monographs, vol 13. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-92679-5_3

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